[Soil Biology] Microorganisms in Soils: Roles in Genesis and Functions Volume 3 || Influence of Microorganisms on Phosphorus Bioavailability in Soils

9 Influence of Microorganismson Phosphorus Bioavailability in SoilsAnnette Deubel1, Wolfgang Merbach1

1Introduction

Phosphorus is the most important plant growth-limiting nutrient in soilsbesides nitrogen. The total phosphorus content of arable soils varies from0.02–0.5% with an average of 0.05% in both inorganic and organic forms(Barber 1995). While most mineral nutrients in a soil solution are presentin millimolar amounts, phosphorus is only available in micromolar quanti-ties or less (Ozanne 1980). This low availability is due to the high reactivityof phosphorus with calcium, iron and aluminum. Alkaline soils containdifferent calcium phosphates like hydroxyapatite and fluoroapatite, whileacidic soils include amorphous iron- and aluminum phosphates, variscite(AlPO4 · 2H2O), strengite (FePO4 · 2H2O) and similar minerals (Barber1995). An important portion of inorganic soil phosphate is adsorbed ontoiron and aluminum oxides and hydroxides, clay minerals and organic sub-stances which contain iron or aluminum complexes. Organic phosphoruscompounds have to be mineralized or enzymatically cleaved to becomeavailable to plants. All these forms are not directly available to plants.

As a result, higher plants depend on diffusion processes and a continuousrelease from insoluble sources to meet their phosphorus demand. As de-composers of organic matter as well as mobilizers of inorganic phosphates– in association and competition with higher plants – soil microorganismsinfluence the availability of phosphorus for plants to a great extent.

2Microbial Effects on Rhizodeposition

As a result of the low phosphorus mobility in soils, plants only have accessto phosphorus a few millimeters around their roots. This volume is highlyaffected by root deposits and intensively settled by microorganisms, which

1Martin-Luther University Halle–Wittenberg, Institute of Soil Science and Plant Nutrition,Adam-Kuckhoff Str. 17b, 06108 Halle, Germany, e-mail: [email protected], Tel:+49-345-5522421, Fax: +49-345-5527113

Soil Biology, Volume 3Microorganisms in Soils: Roles in Genesis and Functions(ed. by F. Buscot and A. Varma)c© Springer-Verlag Berlin Heidelberg 2005

178 A. Deubel and W. Merbach

Table 1. Influence of water-soluble root exudates on double lactate (DL) soluble P 2 mmdistant from the frontage of a loess soil block

Treatment µg DL-P (g soil)–1

Without exudates 1253 days after trickling with 200 mg exudate, sterile 3703 days after trickling with 200 mg exudate, nonsterilea 2703 days after trickling with 320 mg exudate, nonsterileb 432

aAfter 3 days, 75% of 14C was respired by microbesbPlant roots release under nonsterile conditions approx. 60% more exudates in comparisonwith those grown under sterile conditions

use root-borne compounds as energy sources. The rhizosphere effect leadsto an approximately tenfold increase in the microbial population densityin comparison to bulk soil.

A wealth of articles describe the exudation of phosphorus-mobilizingsubstances by plant roots (Johnson et al. 1996; Zhang et al. 1997; Neumannand Römheld 1999; Gaume et al. 2001; Ishikawa et al. 2002). However, neu-tral sugars that sparingly affect P availability occupy the largest part ofwater-soluble root exudates of annual plants (Kraffczyk et al. 1984; Mer-bach et al. 1999; Gransee and Wittenmayer 2000). In addition, such eas-ily decomposable substances are used by microorganisms within a shorttime.

We used water-soluble 14C-labeled maize root exudates containing 80%sugars, 7% amino acids and amides, and 13% carboxylic acids to examinethe phosphorus-mobilizing effect with respect to the concentration gra-dient in the rhizosphere. Freeze-dried excretions were dissolved in waterand trickled onto the front of small soil blocks (20 × 20 × 10 mm Per-spex boxes filled with loess soil, 1.43 g/cm3, 36vol% water content). Theblocks were sealed with paraffin to prevent water loss and incubated at20 ◦C. After 3 days, the blocks were frozen and cut into slices with a cryo-microtome. Root deposits increased the double-lactate soluble P contentof the soil particularly near the trickled area (Schilling et al. 1998). Table 1gives a comparison between sterile (using 60Co for soil sterilization) andnonsterile treatments.

Microbial decomposition of root exudates leads to a smaller increasein phosphorus solubility in comparison to the sterile treatment. If onetakes into account that only one quarter of the radioactivity remains inthe soil after 3 days, these regained substances, which include microbialmetabolites, have a considerably higher specific phosphorus-mobilizingability than the original plant-derived substances. In addition, microbialcolonization increases the exudation rate of plants (Merbach and Ruppel

Influence of Microorganisms on Phosphorus Bioavailability in Soils 179

1992; Meharg and Killham 1995). In general, nonsterile growing plants canusually mobilize more P than sterile growing plants do. The followingparagraph discusses P-mobilizing mechanisms in detail.

3Mechanisms of Microbial Influenceon Phosphorus Availability

3.1Solubilization of Calcium Phosphates

Under alkaline conditions, soil phosphates are fixed in the form of dif-ferent calcium phosphates, mainly apatites and metabolites of fertilizerphosphates. Their solubility increases with a decrease of soil pH.

Phosphorus-mobilizing microorganisms are ubiquitous in soils. Theirdetectable portion among the total microflora depends on soil character-istics as well as on the selection method used. A common simple test isthe use of calcium phosphate-containing agar plates (Whitelaw 2000), onwhich phosphorus-mobilizing colonies produce clear zones. Another pos-sibility is the visualization of a pH decrease using an indicator (Mehta andNautyal 2001). Both methods assume that P release is mainly based on acid-ification of the nutrient medium or the soil. However, the decrease in pH isnot always in the same correlation to the calcium phosphate solubilizationby microorganisms.

To compare the results of different methods, we tested selected rhizo-sphere bacterial strains qualitatively on calcium phosphate agar plates aswell as quantitatively in a liquid medium containing 200 µg P ml−1 in theform of Ca3(PO4)2, 1% glucose and 0.1% asparagine as C and N sources,respectively.

Only two of the eight strains showed clear zones on calcium phosphateagar and could be identified as P solubilizers (Table 2). However, seven ofthe eight strains mobilized significant amounts of tricalcium phosphate.Although some strains acidified the nutrient solution remarkably, we foundno correlation between pH and P in solution. Hence, proton release can-not be the single mechanism of calcium phosphate mobilization. For thisreason, we identified carboxylic anions which are produced under theseconditions (Deubel et al. 2000). We found the following substances in theorder of their amounts:

– D 5/23: succinate, hydroxyglutarate, adipate, lactate, ketogluconate

– PsIA12: succinate, lactate, malate, ketogluconate, galacturonate, cit-rate


Table 2. Phosphorus mobilizing ability of selected rhizosphere bacteriaa

Strain Clear zoneson agar plates

Quantitative estimation ina standing liquid culture(µg P ml–1) pH

D 5/23 Pantoea agglomerans – 62.76 5.93PsIA12 Pseudomonas fluorescens + 44.09 4.77CC 322 Azospirillum sp. – 83.39 6.19Mac 27 Azotobacter chroococcum – 98.11 4.84Ala 27 Azotobacter chroococcum – 1.10 7.50Msx 9 Azotobacter chroococcum – 65.90 5.82ER 3 + 75.48 5.32ER 10 – 36.16 5.72

aIncubation time, 7 days at 28 ◦C; the P content of sterile controls was in the range of2–5 µg/ml at a pH of 6.6–6.9 at the end of incubation time

– CC 322: gluconate, succinate, 2-ketoglutarate, ketogluconate

– Mac 27: citrate, malate, fumarate, succinate, lactate

– Msx 9: citrate, fumarate, malate, lactate, succinate

– ER 10: lactate, gluconate, malonate, citrate

– ER3: fumarate, isocitrate, lactate, malonate

Rhizosphere bacteria are able to produce a broad spectrum of potentialphosphorus-solubilizing substances (Bajpai and Sundara Rao 1971; Banicand Dey 1981; Subba-Rao 1982). Whitelaw (2000) reviewed the productionof oxalate, lactate, glycollate, citrate, succinate and tartrate by differentP-mobilizing fungi. Carboxylic anions, which have a high affinity to cal-cium, solubilize more phosphorus than acidification alone (Staunton andLeprince 1996). Under the same conditions of the experiment above, thefollowing P-concentrations were released from Ca3(PO4)2 by:

– lactic acid: 126 µg P mg−1 = 11.35 µg P µmol−1

– succinic acid: 178 µg P mg−1 = 21.02 µg P µmol−1

– citric acid: 236 µg P mg−1 = 45.34 µg P µmol−1

In some in vitro experiments, proton release seems to be the main mecha-nism of calcium phosphate mobilization (Illmer and Schinner 1995; Villegasand Fortin 2002). However, it should be taken into consideration that nu-trient media often are unbuffered, while soils have effective buffer systems(Whitelaw 2000). Only the proton release in combination with microbialN2 fixation really decreases the pH of alkaline soils. For that reason, car-boxylic anions which mobilize calcium phosphates also in buffered systems


probably have the highest efficiency under natural soil conditions. They of-ten produce insoluble calcium compounds like calcium citrate or oxalate,which may prevent lysing zones on agar plates. Hence, these common testscan fail to detect the really effective microbial strains.

3.2Mobilization of Iron- and Aluminum-Bound Phosphorus

An important potential P source of arable soils is the P fraction adsorbedon iron and aluminum compounds. Carboxylic anions are able to replacephosphate from sorption complexes by ligand exchange (Otani et al. 1996;Whitelaw 2000) and to chelate both Fe and Al ions associated with phos-phate. Citrate for instance, is able to release phosphate from goethite (Geel-hoed et al. 1999) or amorphous ferric hydroxides (Dye 1995). Chelationinvolves the formation of two or more coordinate bonds between a lig-and molecule and a metal ion, thereby creating a ring structure complex(Whitelaw 2000). The ability of different carboxylic anions to desorb P gen-erally decreases with a decrease in the stability constants of Fe (III)- or Al-organic acid complexes (log KAl or log KFe) in the following order: citrate> oxalate > malonate/malate > tartrate > lactate > gluconate > acetate >formiate (Ryan et al. 2001; Whitelaw 2000). The extent to which an organicacid is able to chelate metal cations is greatly influenced by its molecularstructure, particularly by the number of carboxyl and hydroxyl groups.Tricarboxylic acids like citrate have a higher efficiency than dicarboxylic ormonocarboxylic acids. Moreover, the location of groups (α- or β-hydroxyacid structures) can influence the stability of formed complexes.

To demonstrate the P-desorbing efficiency of organic compounds, weextracted P from different slightly acidic soils (pH 5–6) with water, glucoseand ribose (important sugars in root exudates), gluconate, succinate, citrateand oxalate (also possibly released by plant roots directly or produced bymicroorganisms). Figure 1 shows the average of four soils.

Under nonsterile conditions, glucose and ribose released nearly twicethe amount of P as water alone. A neutral gluconate solution was not moreefficient than sugars, and succinate not more than water. In contrast, citrateand oxalate showed an enormous P-mobilizing ability. The P release withcitrate strongly increased within 24 h, but we cannot say whether this isa chemical or microbial effect.

The pH value has controversial effects on P sorption. A proton releaseincreases the availability of iron and aluminum and decreases the negativecharge of adsorbing surfaces, which facilitates the sorption of the alsonegatively charged P ions. However, an acidification leads to an increaseof H2PO−

4 ions in relation to HPO2−4 ions, which have a higher affinity to


Fig. 1. Average of extractable P amounts with different sugars and carboxylic anions atpH 7 (2 g soil was extracted for 1.5 and 24 h with 100 ml solutions containing 5 g/l sugar orcarboxylic acid)

reactive soil surfaces. Therefore, proton release can also decrease P sorption(Whitelaw 2000).

3.3Influence on Phosphorus Diffusion

Carboxylic anions and higher molecular organic substances compete withphosphate for binding sites at adsorbing surfaces. This effect can improvethe diffusion of phosphate ions through the leached zone around plantroots. While the effects of low-molecular compounds are well documented,lack of knowledge still exists concerning the role and composition of mu-cilages in the rhizosphere of higher plants, which may be of both root andbacterial origin. Mucilages are mainly extracellular polysaccharides con-taining, for instance, galactose, fucose and uronic acids (El-Shatnawi andMakhadmeh 2001). They include acidic groups and 1,2 diol polysaccharideresidues. Bacterial mucilages, which are more complex than those of plantorigin, also comprise proteins (Martens and Frankenberger 1991; Watt et al.1993). Gaume et al. (2000) and Grimal et al. (2001) reported a decrease inP adsorption on goethite or ferrihydrite, respectively, by polygalacturonicacid, galacturonic acid and maize root mucilage. In addition to competi-tion for the same adsorption sites, a coating of the minerals by mucilagesis another possible explanation.

Furthermore, mucilages might play an important role in maintainingthe root/soil contact in drying soils (Read et al. 1999). They affect the soilstructure by gluing soil particles together, sometimes producing a sheath


surrounding the roots (Watt et al. 1993; Gregory and Hinsinger 1999). Amel-lal et al. (1999) found a significant aggregation and stabilization of root-adhering soil by bacterial extracellular polysaccharides combined with anincrease in aggregate mean weight, diameter, aggregate macro-porosity,adhering soil: root mass ratio, water-stable > 200 µm aggregates and 0.1–2 µm elementary clayey microaggregates. Watt et al. (1993) reported a 10%higher soil binding capacity of bacterial mucilages in comparison to plantreleased materials.

Phospholipides in root and bacterial mucilages are powerful surfactantsthat alter the interaction of soil solids with water and ions (Read et al.2003). The occupation of adsorption sites as well as influences on aggregatestability and water balance can facilitate phosphorus diffusion processes.

3.4Release of Phosphorus from Organic Sources

Between 20 and 85% of the total P in agricultural soils are present inthe organic form, including inositol phosphate esters, phospholipids, nu-cleic acids, phosphate linked to sugars and derivatives of phosphoric acid(Tarafdar et al. 2001). Microorganisms mineralize organic materials likeplant residues and organic manures and enable the nutrient cycling. Usingan isotopic dilution technique, Oehl et al. (2001) found a daily mineraliza-tion of 1.7 mg P kg−1 in an organically fertilized loamy silt soil. This amountwas approximately equivalent to soil solution P, indicating that mineraliza-tion is a significant process in delivering available P. Although soil solutionscan include higher concentrations of organic than of inorganic phosphates,plants can acquire phosphorus only in inorganic form (Tarafdar et al. 2002).For this reason phosphatases which hydrolyse C–O–P ester bonds are veryimportant for P nutrition. Depending on their pH optimum, acid and al-kaline phosphatases can be determined. Phosphodiesterase, which is ableto degrade nucleic acids, has not been extensively studied in soils (Dodorand Ali Tabatabai 2003). Acid phosphatases are released by plant roots aswell as by microorganisms (Seeling and Jungk 1996; Yadaf and Tarafdar2001), while alkaline phosphatases are probably mostly of microbial origin(Tarafdar and Claasen 1988). The largest portion of extracellular soil phos-phatases is derived from the microbial population and strongly correlateswith microbial biomass (Dodor and Ali Tabatabai 2003). Tarafdar et al.(2001) identified a better hydrolysis of lecithin and phytin by fungal acidphosphatases in comparison to those of plant origin. Glycerophosphatewas equally hydrolyzed by both enzymes. Tarafdar et al. (2002) reportedthat different fungi released only 25% of their acid phosphatases extracel-lularly, but a 39 times higher extracellular phytase activity was noted in


comparison with the one inside the fungal cells. This indicates that fungiespecially can make this important organic P compound available. Thiscorresponds with the results of Hayes et al. (2000) who reported a limiteduse of phytate-P by sterile growing plants.

4Interactions Between Microorganismsand Higher Plants from Competition to Symbiosis

Interactions between microorganisms and higher plants extend from di-rectly detrimental effects of plant pathogens to directly beneficial effectsin the case of symbiosis. Rhizosphere microorganisms can be competitorsfor limited nutrients like P. As a result of higher nucleic acid contents, theyhave higher P concentrations than higher plants. Some microbes are able toincorporate high P amounts in the form of polyphosphates, an energy reser-voir for limited oxygen conditions. Microorganisms often have a higher Puptake efficiency than plant roots. On the other hand, this incorporated Pcan become available to plants as the microbes die. Oberson et al. (2001)reported a rapid microbial P turnover under different land-use conditions.

Plant hormone production by rhizosphere microorganisms can influ-ence root architecture, the development of root hairs and the affinity ofroots for phosphate, indirectly affecting the P uptake.

In particular, different forms of mycorrhiza have great importance forthe P nutrition of higher plants. Most agricultural crops are potential hostplants for arbuscular mycorrhizal (AM) fungi. In addition to an exudationof carboxylates, phosphatases and plant hormones, mycorrhiza increasethe exploitation of the soil volume by the hyphal network, which increasesthe active adsorption surface and spreads beyond the phosphate depletionzone (Lange Ness and Vlek 2000; Martin et al. 2001). Mycorrhizal hyphaehave a higher affinity for phosphate as expressed in the Michaelis-Mentenequation by a lower Km value and absorb P at lower solution concentrationsthan roots do (Lange Ness and Vlek 2000). AM fungi store phosphate inthe form of orthophosphate, polyphosphate and organic P in their vacuolesand transfer it to the roots of the host plant (Ezawa et al. 2002).

5Phosphorus-Mobilizing Microorganisms as Biofertilizers

A great interest in the use of microorganisms as biofertilizers exists espe-cially in areas with a low P availability as a result of an unfavorable soil pH.In addition, inoculates are used to improve the fertilizer efficiency of rock


phosphate (Goenadi et al. 2000; Reddy et al. 2002). Although mycorrhizalfungi are able to improve the phosphorus supply of higher plants morethan other microbes, their use as biofertilizers is complicated because AMfungi, which are able to infect a lot of arable crops, are obligate symbionts.Up-to-date methods for an in vitro production of inocula do not exist. Inaddition, P fertilization depresses the formation of arbuscular mycorrhizas.Therefore, the use of AM inocula is mostly confined to horticulture andrecultivation of mine areas. Much research focuses on bacteria and fungiwhich live in association with higher plants. Some bacterial inoculates canenhance root colonization by mycorrhizal fungi (Ratti et al. 2001).

Although many authors report a growth-promoting effect of phosphorus-solubilizing microorganisms (PSM; (Narula et al. 2000; Sundara et al.2002)), results in the field are highly variable (Gyaneshwar et al. 2002).A yield increase is not always combined with higher P uptake (de Freitas etal. 1997; Deubel et al. 2002; Reyes et al. 2002). The varying success of PSMinoculations can be due to different reasons (Kucey et al. 1989; Gyaneshwaret al. 2002): (1) insufficient survival and colonization of inoculated strains,(2) competition with native microorganisms, (3) nature and properties ofsoils and plant varieties, (4) starvation of nutrients in the rhizosphere toproduce enough organic acids to solubilize soil phosphates and (5) inabilityof PSMs to solubilize soil phosphates.

Because of the ubiquitous occurrence of phosphorus-mobilizing mi-crobes, a yield increase by inoculation with additional strains may bebeneficial if these organisms possess different growth-promoting abilities,for instance N2 fixation, phytohormone production and phosphorus mo-bilization (Peix et al. 2001). One of the greatest problems is insufficientselection and test methods for phosphorus-mobilizing microorganisms.The selection on clear zones or a pH decrease in simple plate tests cannotreflect the real P binding capabilities under soil and rhizosphere conditions.A better possibility may be the selection of microbes, which can effectivelyuse P adsorbed on goethite or other minerals (He et al. 2002). Becausemany more microbes have the ability to solubilize phosphates under spe-cial conditions than to colonize and promote growth of higher plants, itis useful to select first on the basis of growth-promoting abilities. A lim-ited number of strains can then be tested for special properties. It mustbe taken into account that test conditions influence the results to a largeextent. A given strain can respire a sugar to CO2 under high oxygen supply,or produce carboxylic acids by fermentation or incomplete respiration ifoxygen is limiting. Moreover, the type of C sources affects the productionof microbial metabolites (Kim et al. 1998; Deubel et al. 2000).

We tested the influence of different sugars on the Ca3(PO4)2-mobilizingefficiency of different bacterial strains. Figure 2 shows a comparison ofglucose, which represents a large portion of water-soluble root exudates of


Fig. 2. P release from Ca3(PO4)2 by different bacterial strains with glucose or ribose asC source (standing liquid culture 7 days at 28 ◦C, 4 mg C ml−1 as sugar, 200 µg P ml−1 asCa3(PO4)2)

well-nourished plants, with ribose, which is present in increasing amountsunder P deficiency (Deubel et al. 2000).

Although all strains were able to grow with both sugars as the C source,Pantoea and Azospirillum increased P mobilization with ribose, while otherstrains released less or no phosphate with this sugar. These changes in P-mobilizing ability were combined with changes in the pattern of producedcarboxylic acids. The same results were found in the response of differentbacteria on synthetically mixed root exudates of well-nourished and P-deficient plants (Fig. 3).

Fig. 3. Influence of synthetic sugar mixtures [in analogy to the saccharide portion of rootdeposits of Pisum sativum plants with P (pea exudates + P) and without P supply (peaexudates – P)] in comparison to standard medium (glucose) on the Ca3(PO4)2 solubilizingability of the bacterial strains D 5/23, PsIA12 and CC 322


Therefore, it is very important to consider the real conditions in therhizosphere of potential host plants during the test procedure.

Another issue is the demand of C sources to produce carboxylic acidsin sufficient amounts. A symbiotic relation with higher plants, for instancemycorrhiza or rhizobia symbiosis (Vance 2001), can best provide enoughorganic C compounds for P-mobilizing processes. On the other hand, onlya few substances, particularly citrate and oxalate are effective in micromolarconcentrations, which are realistic for rhizosphere conditions. Hence, it isuseful to look for producers of such effective substances, for instance bygenetic characterization (Igual et al. 2001).

One possibility to increase the P-mobilizing efficiency of microbialstrains is the induction of mutations by UV light (Reyes et al. 2001), orchemical substances (Narula et al. 2000), as well as genetic manipulation(Gyaneshwar et al. 1998; Rodriguez et al. 2000). However, the chances andrisks in the spreading of genetically modified microorganisms have to beweighed carefully.

Soil microorganisms have an enormous potential to improve phospho-rus bioavailability. A better understanding of the interactions betweendifferent microorganisms as well as between microorganisms and higherplants, improved selection and test procedures and the development ofculture methods for mycorrhizal fungi will help to realize this potential asbiofertilizers.

6Conclusions

Soil microorganisms, particularly the rhizosphere flora of higher plants,remarkably affect the phosphorus bioavailability in soils. Microbially de-rived carboxylic acids mobilize calcium phosphates as well as iron- andaluminum-bound phosphorus. Microbial mineralization of organic matteris essential for nutrient cycling in soils and phosphatases enhance the use oforganic P compounds by higher plants. Plants, especially in nutrient-poorhabitats like forest ecosystems, often depend on symbiotic relations withmicroorganisms like mycorrhizal fungi. However, rhizosphere flora alsodecomposes P-mobilizing substances derived from plant roots. Microor-ganisms can be powerful competitors for growth-limiting nutrients like P,but microbial turnover can also make P available for higher plants. The dif-ficulty in quantifying all these complex and partially contrary processes isa substantial weak point in mathematical P-utilization models as well as inthe use of P-mobilizing microbes as biofertilizers. The investigation of thesecomplex effects with modern methods, which cover also the large majorityof noncultivable microorganisms, is an important aim for further research.


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Part IVBiotic Interactions Involving Soil Microorganisms

Documents

[Soil Biology] Microorganisms in Soils: Roles in Genesis and Functions Volume 3 || Influence of Microorganisms on Phosphorus Bioavailability in Soils